Research paper- Diclofenac Poisoning of Vultures in South Asia: The Race to Save Avian Scavengers

Abstract

            Vultures play a critical role in ecosystems as the only obligate vertebrate scavengers. They are also the most threatened avian functional group in the world. In this case study, I trace the dramatic example of vulture decline throughout South Asia in order to elucidate the causes, effects, and response to this international crisis. Over the course of two decades, three related species of vulture, the white-rumped vulture (Gyps bengalensis), the slender-billed vulture (Gyps tenuirostris), and the Indian vulture (Gyps indicus) went from millions of individuals to just a few thousand. Thanks to collaboration between scientists, NGOs, and governments across multiple nations, these species have been saved from the brink of extinction. Efforts to protect vultures included the discovery of what caused the declines (a veterinary drug called diclofenac), research into a viable alternative medication, a subsequent ban on diclofenac, and captive breeding activities. Despite important wins, however, the fight to save vultures throughout Asia is far from done. Continuing challenges include other poisonous veterinary drugs and the continued use of diclofenac itself in South Asia and beyond. Critical conservation lessons can be gleaned from this ongoing project, including the importance of collaboration, the power of culture to motivate change, and the need for constant vigilance—as even the most abundant species can be threatened by unforeseen circumstances.

Diclofenac Poisoning of Vultures in South Asia:

The Race to Save Avian Scavengers

            According to the International Union for Conservation of Nature (IUCN), approximately 224 bird species are critically endangered worldwide, with an additional 469 are listed as endangered (IUCN, 2019). Given the variety of critical roles birds play in nature, as well as their intrinsic, economic, and cultural value, the conservation of birds facing extinction is an issue of immediate concern for the global community. Over the past three decades, one particular group of birds has experienced the most rapid and catastrophic declines in recent history. Vultures, the only obligate vertebrate scavengers, now make-up the most threatened avian functional group in the world (Buechley & Şekercioğlu, 2016).

            The functional group “vulture” is comprised of 22 different species of great geographic and taxonomic diversity, united by a shared ecological niche. As obligate scavengers, these birds gain a vast majority of their caloric intake through scavenging behaviors (Buechley & Şekercioğlu, 2016; Prakash et al., 2003). This makes them foundational species in many of the ecosystems in which they occur, often referred to as “keystone” species (Markandya et al., 2008). Unfortunately, of these 22 important species, nine are critically endangered and three are endangered. All of these endangered species are thought to be still actively decreasing as of 2019, with the exception of the California condor (IUCN, 2019).

Although there are a variety of threats facing vultures, including habitat loss, climate change effects, and hunting, at least half of all vulture species are threatened by environmental toxins specifically (IUCN, 2019). DDT (Dichlorodiphenyltrichloroethane) infamously decimated North American raptor populations in the mid-twentieth century, including the California condors. In her seminal Silent Spring, Rachel Carson outlined the dangers posed by this pesticide. As a result of her work and others’, DDT was banned, but other toxins persist and have been introduced since. These include lead, other pesticides and herbicides, and even pharmaceuticals (Tubbs, 2016).

In recent years, one such contaminant known as diclofenac has caused an unprecedented population decline in several species of Asian vultures (Green, et al., 2004). In the present case study, I will outline this example of a catastrophic population loss in response to a human-introduced toxin. By examining the crisis, the subsequent response, and current status of this issue, I will elucidate what lessons can be gleaned from this modern conservation dilemma.

Description of Species

            The Indian sub-continent is home to nine to ten species of vultures. Four to five (depending on accepted taxonomy) of these vultures are considered to be in the genus Gyps. Gyps are found across Asia, Africa, and Europe, are obligate scavengers, and typically breed colonially. As recently as the 1980s, Gyps vultures were exceedingly common in South Asia. However, throughout the 1990s and continuing into this century, several species of Gyps experienced a sudden and catastrophic decline (Buechley & Şekercioğlu, 2016; Prakash et al., 2003). This case study will focus on the three species of vulture known to have been nearly destroyed during this period. These are the white-rumped vulture (Gyps bengalensis), the slender-billed vulture (Gyps tenuirostris), and the Indian vulture (Gyps indicus) (Green et al., 2004).

            The white-rumped vulture was once considered to be the most abundant raptor in the world (Prakash, et al., 2019). They are the smallest of the Gyps genus, but still sizeable birds, with a wingspan of 1.92–2.6 meters (Rasmussen and Anderton, 2005). They had the widest range of the three vultures most severely affected by diclofenac, and once occurred throughout India, Pakistan, and much of Southeast Asia. Today, their populations have declined by over 99%, with only a few thousand individuals believed to still exist, spread throughout South Asia (Prakash et al., 2007).

            The Indian vulture was once considered to be the same species as the slender-billed vulture. More recent evidence suggests they are distinct species, though they are very similar in terms of coloring, size, and behavior (Prakash et al., 2003). The Indian vulture, as its name suggests, is native primarily to the Indian sub-continent, while their slender-billed cousins are typically found in northern India, Bhutan, Bangladesh, and Southeast Asia. Like the white-rumped vulture, they were once exceedingly numerous, with millions of individuals thought to exist. During the Indian vulture crisis, their populations dropped by more than 95% (Prakash, 1999).

            Given their role as obligate scavengers, this dramatic loss of these three Gyps species had immense ecological consequences. However, vultures have value beyond their environmental role. To best understand the full cost of these near-extinctions, it is critical to first understand the spiritual and cultural value of vultures in this part of the world.

Cultural Context

            Perhaps due to their historical ubiquity, depictions of vultures are common throughout South Asian cultural works including, art, writings, and spiritual practices (Haas & Mundy, 2013; Bindra, 2018). They are particularly prominent in Hindu traditions. Considered the world’s third-most common religion, Hinduism has existed throughout South Asia for thousands of years. Vultures play a prominent role in aspects of this ancient spiritual path, reflecting their cultural importance. Most famously, the vulture god Jatayu appears in a heroic role in the sacred text of the Ramayana—one of Hinduism’s foundational works. In this epic, Jatayu gives his life to protect Sita, a demi-goddess and princess who is the Ramayana’s main female figure. As a result, Jatayu is seen as a symbol for the protection of women and is honored by the Jatayu Earth Center in the form of a massive sculpture—the largest bird monument in the world (Haas & Mundy, 2013). Jatayu’s brother, Sampati, is also a figure in the Ramayana, wherein he assists those searching for Sita by providing information on her whereabouts (Kushwaha, 2016). Although not completely positive—as Sampati threatened to eat the heroes before he learned of his brother’s sacrifice—these two mythic vultures demonstrate the cultural importance of vultures to those who follow Hinduism.

            Besides their presence in Hindu teachings, vultures play a critical role in other spiritual practices. One such example is the funerary ritual known as “sky burial.” This tradition involves the offering of loved ones’ bodies to be consumed by vultures and other carrion birds. This practice is not followed by one path exclusively. Rather, followers of certain sects of Tibetan Buddhism and Zoroastrianism utilize this method (Martin, 1996).

While its exact history and prevalence in Tibetan Buddhism is debated, one of the earliest descriptions of sky burials in Tibet is provided by a travelling friar from the early 1300s.

“Then the priest cuts the whole of the body to pieces…After this, the eagles and the vultures come down from the mountains, and every one takes his morsel…”

(Martin, 1996)

            Accounts of Buddhist sky burials have also been reported in China, Bhutan, and Mongolia. Seen as an inferior and insulting practice by China’s Manchu court, the practice was banned in the 18th century. However, despite the threat of capital punishment, it appears that this edict had little effect on the continued engagement with this ritual (Martin, 1996).

            Sky burial is also practiced by members of the Zoroastrian faith. This ancient religion originated in Persia (modern-day Iran), and reports of sky burial practices extend into antiquity, with accounts from Herodotus, Cicero, and more (Martin, 1996). Parsi people have since migrated throughout Asia and the world, resulting in communities of Zoroastrians practicing sky burial in parts of modern India. Given the similarity of these funerary practices across Tibetan Buddhism and Zoroastrianism, some speculate that perhaps these traditions are related—with one pre-dating and influencing the other. However, there is little evidence to support or refute this theory (Martin, 1996).

            Another idea about the origins of this practice relates to the local ecology and geography, of the sub-Himalayan region. From this perspective, the practice of dismembering bodies and allowing them to be quickly consumed by efficient avian scavengers can be seen as an adaptive cultural response to environmental limitations, including limited arable land and shortage of fuel sources. Essentially, by allowing vultures and other carrion-feeders to break-down corpses, land that would otherwise be taken up by graves could instead be utilized for farming and fuel that would otherwise be needed for cremation could be conserved for other purposes (Martin, 1996). In an interesting parallel, the Tibetan god Nyen rules over mountains, and is offended by the digging of land and cutting of trees, providing an additional taboo against over-use of land and harvesting of fuel (Vigoda, 1989). Vultures are clearly an important part of this ancient practice, and indeed their health and safety are taken into consideration when deciding whether to give the decedent a sky burial or not. Individuals thought to have died of disease or poisoning are buried instead, out of fear that the birds might be harmed and the disease may be spread (Martin, 1996).

            Inherent in these traditions, and many other Asian spiritual beliefs, is an understanding of the interconnectedness of humans and the natural world (Vigoda, 1989). This ecological reality is imprinted within cultural practices, but can also be understood from a scientific perspective. In addition to their primarily positive depictions in South Asian culture and religion, vultures are recognized by the scientific community as a critical part of a healthy ecosystem (Markandya et al., 2008). 

The Ecological and Health Importance of Vultures in South Asia

            Scavenging is a fairly common foraging strategy for a variety of animals. Most vertebrate species that engage in scavenging do so as part of a larger array of foraging techniques, and are therefore known as “facultative” scavengers. These can include omnivorous and predatory mammals like canids, and birds such as corvids and gulls (Buechley & Şekercioğlu, 2016). Obligate scavenging is far rarer, with vultures being the only known obligate vertebrate scavengers in the world. As a result, when it comes to carrion removal, vultures are critically important for the breakdown of soft tissues that might otherwise fester and cause disease (Prakash et al., 2003). Globally, vultures consume a significant amount of all available carrion due to their highly specialized adaptations for this spatially and temporally unpredictable food source. These include soaring flight that gives them advantage over terrestrial scavengers and bald heads that prevent build-up of carrion remnants. Indeed, in some parts of the world, vultures are responsible for the clean-up of 90% of all carrion (Buechley & Şekercioğlu, 2016).

            Given their historical prevalence in South Asia and their evolutionary advantages over facultative competitors, it is not surprising that, until recently, vultures like the Indian, white-rumped, and slender-billed comprised the majority of scavengers in the area (Prakash et al., 2003). Their large numbers (comprised of millions of birds) and superior ability to locate ephemeral carrion sources is thought to have given them significant advantages over their main competitors for carrion—jackals and feral dogs. From a community ecology lens, this meant that large numbers of vultures effectively lowered the carrying capacity for jackal and feral dog populations (Markandya et al., 2008).

            This competitive exclusion interaction has significant implications for human health as well. Due to the cultural significance of cows in Hinduism and taboos against the removal of carcasses, massive amounts of cow carrion is present within and very near human communities (Markandya et al., 2008; Prakash et al., 2007). This, combined with other attractants such as trash, results in massive amounts of scavengers being drawn into close proximity with humans. Since mammalian scavengers like jackals and especially feral dogs are capable of carrying several zoonotic diseases, their presence is particularly dangerous. Dogs are the number one transmitter of rabies—a fatal and devastating disease—worldwide, and also spread a variety of harmful parasites. On the other hand, birds like vultures transmit relatively few diseases to humans as a result of being more removed morphologically and taxonomically from our species. Put simply, more vultures meant fewer canids, which resulted in decreased risk of disease transmission (Markandya et al., 2008). Just as Jatayu protected Sita, the presence of large vulture populations can act as a buffer against devastating diseases.

            Given their foundational role as obligate scavengers and links to protecting public health, it is clear why vultures are considered to be critical to healthy ecosystems and communities. So, when South Asian vultures mysteriously began dying off at an alarming rate beginning in the 1990s, this created an international crisis that would require a swift and powerful response.

The Asian Vulture Crisis

            Dr. Vibhu Prakash, a world-renowned raptor biologist, is largely credited for the initial discovery of massive Gyps vulture declines. In his work throughout the 1980s and 1990s, Dr. Prakash studied vulture populations in Keoladeo National Park, finding massive numbers of dead or sickened vultures with a characteristic “neck droop.” By the time Dr. Prakash published his initial study, three species of Gyps vultures faced extinction. White-rumped vultures had lost an estimated 99% of their population, while the Indian and slender-billed varieties were down an estimated 97% (Prakash, 1999; SAVE, 2019). The situation was dire—but it was not yet clear what was causing these massive die-offs.

            Several hypotheses were investigated by scientists funded by a variety of sources including the Peregrine Fund, the Darwin Initiative, and the Royal Society for the Protection of Birds (Watson, Gilbert, Oaks, & Virani, 2004). Potential explanations for the decline included a new avian disease, habitat loss, food shortages, and environmental toxins (Prakash et al., 2003). By the early 2000s, scientists narrowed down the list of potential causes to a non-steroidal anti-inflammatory (NSAID) drug called diclofenac (Green et al., 2004).

            First suspected due to correlation between the drug’s introduction and the beginning of vulture declines, diclofenac was officially confirmed as the mystery threat to vultures in 2004 (Green et al., 2004). In this initial study conducted in Pakistan, researchers found evidence of diclofenac poisoning in deceased Gyps vultures leading to a build-up of uric acid (Oaks et al., 2004). Subsequent follow-up studies in India, Nepal, and Bangladesh confirmed this pattern, revealing the main cause of the massive vulture declines after almost one-and-a half decades (Green et al., 2004; Watson et al., 2004; Taggart et al., 2007).

            Unfortunately, identifying the cause of this unprecedented loss of vultures was only the first important challenge that had to be addressed. Once diclofenac’s deleterious effect on vultures was proven, the individuals and organizations working to save Gyps vultures from extinction had to turn their attention to removing this threat from the environment and preserving what few vultures remained.

The Objectives

            When it came to saving the Indian, white-rumped, and slender-billed vultures, there were multiple critical objectives. In order to decrease—and ideally eliminate—the use of diclofenac in livestock that might be consumed by vultures, those prescribing and using the drug had to be educated about its harmful effects, and be provided with a viable alternative to keep their cattle comfortable. At the same time, the few thousand individual Gyps vultures still living in South Asia had to be protected as much as possible. Finally, a robust captive-breeding program would be necessary to ensure a future for these three species. To realize these goals, buy-in from a wide array of stakeholders, including governments, NGOs, scientists, civilians, and businesses was needed (SAVE, 2019).

Procedures

            To meet these objectives and organize the interested parties, twenty-four partner organizations came together, eventually forming SAVE (Saving Asia’s Vultures from Extinction). One of vulture advocates’ first major milestones came in 2004, where meetings in India and Nepal resulted in the creation of the Diclofenac Manifesto and the Vulture Recovery Plan. These formal documents pledging support for ridding South Asia of diclofenac residue and actively working to recover vulture populations were signed by both Indian and Nepalese NGOs and international NGOs (SAVE, 2019). Moreover, these plans had the support of their national governments. Specific pledges included working to ban diclofenac for veterinary use, finding a viable, vulture-safe alternative, and establishing captive breeding centers (Swan et al., 2006).

            That same year, the first vulture conservation breeding center was established in Pinjore, Haryana State, India. Several more centers opened in India and Nepal in subsequent years, and turned their attention to attempting to successfully breed the three endangered Gyps vultures in captivity for the first time (SAVE, 2019). As raptor biologists focused on repopulation efforts, other scientists took on the task of finding a vulture-safe NSAID that could be used in veterinary settings instead. After surveying raptor-keepers worldwide and extensive safety testing, researchers found a newer drug, meloxicam, that did not produce the deadly build-up of uric acid in vultures (Swan et al., 2006).

            In parallel to the important work being conducted by scientists, members of SAVE also partnered with the Indian government. India’s Ministry of Environment and Forests created their own vulture action plan in 2006. In keeping with this plan, veterinary diclofenac was banned in India. Nepal and Pakistan soon followed suit, representing a serious commitment to making the environment safe for vultures again (Nambirajan et al., 2018).

            Vulture research centers also established education campaigns, primarily aimed at school-aged children, with the hope that kids would then tell their parents about the dangers of diclofenac. Advocates also put up flyers and posters, in order to increase public awareness of the ban, as well as support. To further promote compliance with the law, the government stiffened the punishment to include jail-time for those that illegally used veterinary diclofenac (SAVE, 2019).

            Throughout the 2000s and 2010s, the quest to save Asia’s vultures gathered even more support. Together with the IUCN, the Indian government called a meeting of several South Asian countries, leading to a Regional Declaration signed by Bangladesh, Nepal, India, and Pakistan. Vulture-safe zones were also created to provide safe places for the few remaining wild vultures. As part of the international collaborative efforts, researchers who had successfully created such zones held workshops to teach others to do the same (SAVE, 2019). This included the opening of “vulture restaurants,” such as Jatayu vulture restaurant in India, where diclofenac-free carcasses are collected to attract vultures to a safe food source (Decandido, Subedi, & Allen, 2012).

            The effort to save Gyps vultures led to the formation of several important partnerships and many critical steps to try and reverse this unprecedented decline. But, were these efforts successful? Given the loss of over 97% of the population, full recovery is still a long way away, but the work of scientists, NGOs, and governments has led to many positive results.

Results

            In 2008, two white-rumped vulture chicks were born in captivity for the very first time. Within only a few years, all three species of endangered Gyps vultures were successfully bred in captivity. By 2014, breeding centers were producing up to 35 fledglings a year as they learned more about what strategies worked best for rearing these species (SAVE, 2019). Although these numbers may seem small, they represent a future for these species that might otherwise have been lost.

            Although the response to diclofenac’s ban was lukewarm at first, several important changes led the level of diclofenac-poisoned carcasses and vultures to fall substantially—from 11% to 6% and from 43% to 18% respectively. These changes included the release of meloxicam’s patent by German manufacturer Boehringer Ingelheim, allowing more affordable generic versions to be made available. The sale of multi-use bottles of diclofenac that could be used to illegally treat livestock was also banned in 2015, in an effort to further reduce ban violations (“Ban,” 2015; SAVE, 2019). Investigations into the presence of veterinary diclofenac in retail stores showed that it was absent or very scarce throughout Nepal and India. These policy changes and results so far bode well for the elimination of veterinary diclofenac throughout Nepal and India in the near-future. However, despite these exciting changes, the fight to save vultures is far from over (SAVE, 2019).

Current Status and Continuing Challenges

            Thanks to the dedication and hard work of researchers like Dr. Vibhu Prakash, organizations like the Peregrine Fund and Darwin Initiative, and national governments, incredible strides have been made in addressing the Asian vulture crisis. Unfortunately, their efforts have also led to the discovery of new and continuing barriers to vulture recovery. Although compliance with diclofenac bans has increased substantially, it is still being utilized illegally throughout South Asia (Cuthbert et al., 2016; SAVE, 2019). Moreover, in the years since the discovery of diclofenac’s toxicity to vultures, several other NSAIDS have been found to be equally dangerous (Bindra, 2018). Meloxicam is considered the only veterinary NSAID safe for vultures, and continued efforts focus on ensuring children and their parents are aware of this (Cuthbert et al., 2016; Swan et al., 2006). Diclofenac and other NSAIDS remain a threat to any vultures living in the wild, underlining the importance of vulture restaurants/safe zones and captive breeding programs (Cuthbert et al., 2016).

            Although the loss of Gyps vultures throughout South Asia is the most dramatic decline, nine other species of vultures are endangered worldwide (IUCN, 2019). As evidenced by the sudden loss of millions of Indian vultures, even vulture species considered to be of least concern are at risk if diclofenac and other toxins are allowed to remain in the ecosystem. While diclofenac is banned across multiple countries in South Asia, it was recently approved for veterinary use in Europe (Camiña, Aguilera, Sarrazin, & Duriez, 2019). Currently, organizations including BirdLife Europe and the Vulture Conservation Foundation are campaigning to ban diclofenac in Europe. Their efforts are specifically focused on Spain and its surrounding nations, since a vast majority of Europe’s vultures, including threatened bearded vultures (Gypaetus barbatus) are found there (Margalida et al., 2008; “New Campaign,” 2017). Only time will tell if these efforts will be successful, or if Europe’s vultures might be headed for collapse as South Asia’s did.

Lessons Learned and Conclusions

            When it comes to parsing out what conservation lessons can be learned from this case study, the first important factor to understand is the power of successful collaboration. No single group of stakeholders—scientists, NGOs, or national governments—could have made all the strides in protecting Asia’s vultures alone. The abundant success of this initiative can likely be traced to formal partnerships, like those created under the SAVE banner, where various collaborators across multiple countries pledged to do their part to protect vultures. The continued annual meetings, new discoveries, and updated goals that SAVE produces can serve as an excellent example of an international conservation collaboration (SAVE, 2019).

            Beyond the importance of such powerful alliances, this case study demonstrates how cultural significance can be capitalized upon to increase buy-in from local communities. The decision to name the first vulture restaurant after Jatayu—the heroic spiritual figure—was likely not an accident (Decandido et al., 2012). Indeed, by making this conscious connection, vulture advocates remind their peers about this ancient connection. Multiple scientists also cite the cultural and religious significance of vultures in their publications, as a critical rationale for the conservation of these threatened scavengers (Prakash et al., 2003; Ogada, Keesing, & Virani, 2012).

            Collaboration and cultural mobilization are key lessons from this case study, but perhaps the most important and haunting message of all is the fragility of even the most abundant populations. Like the infamous passenger pigeon once said to be so numerous their flocks blocked the sun, the white-rumped vultures were the most abundant raptor in the world as recently as the 1980s (Prakash et al., 2019). If it weren’t for the vigilance and dedication of the individuals and organizations involved in saving Asian vultures, the white-rumped vultures and their other Gyps cousins may well have shared the same fate at the extinct passenger pigeon. This case therefore is a cautionary tale that reminds us not to take species for granted simply because they are currently numerous. Even the most common of animals can be threatened when something new is introduced into their ecosystem. So, while endangered and threatened species rightly take up much of the world’s attention and conservation resources, it is important that we seek to preserve and protect common species as well.

            The white-rumped, slender-billed, and Indian vultures could easily have gone the way of the passenger pigeon, great auk, and other once abundant, now extinct, birds of the past. Instead, thanks to timely action by individual researchers, governmental bodies, and significant international collaboration, the future for Gyps vultures in South Asia is promising. While they may never reach their pre-diclofenac numbers in our lifetime, these magnificent raptors will continue to grace the skies of Asia for generations to come.

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